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Richard Bireley, Shannon Borges, Karina Cham, David Epstein, Kristina Garber, Connie Hart, Wayne Hou, Alessio Ippolito, Jens Pistorius, Veronique Poulsen, Keith Sappington, Thomas Steeger
Natalie K. Boyle, Theresa L. Pitts-Singer, John Abbott, Anne Alix, Diana L. Cox-Foster, Silvia Hinarejos, David M. Lehmann, Lora Morandin, Bridget O'Neill, Nigel E. Raine, Rajwinder Singh, Helen M. Thompson, Neal M. Williams, Thomas Steeger
Current pesticide risk assessment practices use the honey bee, Apis mellifera L., as a surrogate to characterize the likelihood of chemical exposure of a candidate pesticide for all bee species. Bees make up a diverse insect group that provides critical pollination services to both managed and wild ecosystems. Accordingly, they display a diversity of behaviors and vary greatly in their lifestyles and phenologies, such as their timing of emergence, degree of sociality, and foraging and nesting behaviors. Some of these factors may lead to disparate or variable routes of exposure when compared to honey bees. For those that possess life histories that are distinct from A. mellifera, further risk assessments may be warranted. In January 2017, 40 bee researchers, representative of regulatory agencies, academia, and agrochemical industries, gathered to discuss the current state of science on pesticide exposure to non-Apis bees and to determine how well honey bee exposure estimates, implemented by different regulatory agencies, may be protective for non-Apis bees. Workshop participants determined that although current risk assessment procedures for honey bees are largely conservative, several routes of exposure are unique to non-Apis bees and warranted further investigation. In this forum article, we discuss these key routes of exposure relevant to non-Apis bees and identify important research gaps that can help inform future bee risk assessment decisions.
Angela E. Gradish, Jozef van der Steen, Cynthia D. Scott-Dupree, Ana R. Cabrera, G. Christopher Cutler, Dave Goulson, Olaf Klein, David M. Lehmann, Johannes Lückmann, Bridget O'Neill, Nigel E. Raine, Bibek Sharma, Helen Thompson
To date, regulatory pesticide risk assessments have relied on the honey bee (Apis mellifera L.) (Hymenoptera: Apidae) as a surrogate test species for estimating the risk of pesticide exposure to all bee species. However, honey bees and non-Apis bees may differ in their susceptibility and exposure to pesticides. In 2017, a workshop (‘Pesticide Exposure Assessment Paradigm for Non-Apis Bees’) was held to assess if honey bee risk assessment frameworks are reflective of non-Apis bee pesticide exposure. In this article, we summarize the workshop discussions on bumble bees (Bombus spp.). We review the life history and foraging behavior of bumble bees and honey bees and discuss how these traits may influence routes and levels of exposure for both taxa. Overall, the major pesticide exposure routes for bumble bees and honey bees are similar; however, bumble bees face additional exposure routes (direct exposure of foraging queens and exposure of larvae and adults to soil residues). Furthermore, bumble bees may receive comparatively higher pesticide doses via contact or oral exposure. We conclude that honey bee pesticide risk assessments may not always be protective of bumble bees, especially queens, in terms of exposure. Data needed to reliably quantify pesticide exposure for bumble bees (e.g., food consumption rates, soil residue levels) are lacking. Addressing these knowledge gaps will be crucial before bumble bee exposure can be incorporated into the pesticide risk assessment process. Because bumble bees exhibit appreciable interspecific variation in colony and behavioral characteristics, data relevant to pesticide exposure should be generated for multiple species.
Fabio Sgolastra, Silvia Hinarejos, Theresa L. Pitts-Singer, Natalie K. Boyle, Timothy Joseph, Johannes Lūckmann, Nigel E. Raine, Rajwinder Singh, Neal M. Williams, Jordi Bosch
Current pesticide risk assessment for bees relies on a single (social) species, the western honey bee, Apis mellifera L. (Hymenoptera: Apidae). However, most of the >20,000 bee species worldwide are solitary. Differences in life history traits between solitary bees (SB) and honey bees (HB) are likely to determine differences in routes and levels of pesticide exposure. The objectives of this review are to: 1) compare SB and HB life history traits relevant for risk assessment; 2) summarize current knowledge about levels of pesticide exposure for SB and HB; 3) identify knowledge gaps and research needs; 4) evaluate whether current HB risk assessment schemes cover routes and levels of exposure of SB; and 5) identify potential SB model species for risk assessment. Most SB exposure routes seem well covered by current HB risk assessment schemes. Exceptions to this are exposure routes related to nesting substrates and nesting materials used by SB. Exposure via soil is of particular concern because most SB species nest underground. Six SB species (Hymenoptera: Megachilidae - Osmia bicornis L., O. cornifrons Radoszkowski, O. cornuta Latreille, O. lignaria Say, Megachile rotundata F., and Halictidae - Nomia melanderi Cockerell) are commercially available and could be used in risk assessment. Of these, only N. melanderi nests underground, and the rest are cavity-nesters. However, the three Osmia species collect soil to build their nests. Life history traits of cavity-nesting species make them particularly suitable for semifield and, to a lesser extent, field tests. Future studies should address basic biology, rearing methods and levels of exposure of ground-nesting SB species.
Karina O. Cham, Roberta C. F. Nocelli, Leandro O. Borges, Flávia Elizabeth C. Viana-Silva, Carlos Augusto M. Tonelli, Osmar Malaspina, Cristiano Menezes, Annelise S. Rosa-Fontana, Betina Blochtein, Breno M. Freitas, Carmen Silvia S. Pires, Favízia F. Oliveira, Felipe Andres L. Contrera, Karoline R. S. Torezani, Márcia de Fátima Ribeiro, Maria A. L. Siqueira, Maria Cecília L. S. A. Rocha
Although the importance of bees as the pollinators responsible for maintaining gene flow for many native and cultivated plants in ecosystems around the world is recognized, much of their biodiversity and behavior remains to be discovered. Stingless bees are considered key pollinators for several plant species in tropical and subtropical ecosystems and they also provide pollination services for economically important agricultural crops. Many countries are using the honey bee (Apis mellifera Linnaeus, 1758, Hymenoptera: Apidae) as a surrogate to evaluate the risk of pesticides to all species of bees. However, there is uncertainty regarding the extent to which honey bees can serve as surrogates for non-Apis bee species in the risk assessment for pesticides. This paper provides a short overview of the life history traits relevant in risk assessment of stingless bees. It summarizes what is known about stingless bee exposure to pesticides compared to that of honey bees and presents criteria for potential candidate species from Brazil for use in pesticide risk assessment in tropical environments. This paper also identifies gaps in knowledge of bee biology and pesticide exposure routes not covered by the current honey bee exposure assessment paradigm. Based on these gaps, research is needed on life history traits, estimates of nectar and pollen consumption, mud, resin, and water collection and available protocols to adequately assess toxic effects of pesticides to stingless bees. This review is part of a series of papers on the risk of exposure of non-Apis bees to pesticides.
Fern–insect interactions have not received the same attention as angiosperm–insect interactions have. It has even been stated that ferns may have very few interactions with animals because of their lack of flowers, fruits, and seeds. Consequently, for many decades fern–insect interactions have been overlooked and underestimated, especially for highly developed interactions such as those with gall-formers. The present work aims to review the galls of ferns and lycophytes worldwide, to provide an updated checklist including unpublished data and to estimate the global gall diversity of ferns and lycophytes. We recorded 93 host species, belonging to 41 genera. Galls were found in 20 fern families and one lycophyte family (Selaginellaceae). Most galls occur within the more derived ferns of the order Polypodiales, especially the fern families Polypodiaceae (21 host species), Dryopteridaceae (14 host species) and Athyriaceae (11 host species).Thirty-eight of the 133 gall morphotypes were induced by mites and 95 by insects of six orders (Coleoptera, Diptera, Hymenoptera, Lepidoptera, Thysanoptera, and Hemiptera). Among the insects, Cecidomyiidae (Diptera) caused most of the galls (35 morphotypes). So far, most galls have been reported from the Neotropical region (40 spp.) and Oriental region (28 spp.).
Interspecific interactions are influenced by several environmental factors that may affect spatial and temporal dynamics. Seasonal variations in environmental conditions and differences among sites may affect the intensity of interactions and the abundance of interacting species. In this study, we describe the variability in parasitoids of Atta ants among sites and seasons over a year. More specifically, we studied parasitoidism of Atta sexdens Linnaeus and Atta laevigata Smith nests at a site with native cerrado vegetation and a Eucalyptus monoculture in dry and rainy seasons. Of the 45,147 workers collected, 1,020 (2.2%) were parasitized. We found five parasitoid species of A. sexdens and four species of A. laevigata. The two species of leaf-cutting ants shared similar parasitoid communities, but the infection rate was higher in A. laevigata (5.3%) compared with A. sexdens (0.8%). Parasitoidism rates of A. laevigata increased in the rainy season, but the rate for A. sexdens was consistently low in both seasons. The identity of the host species and the season, therefore, appear to interact to influence the rate of parasitoidism in these leaf-cutting ant species.
The invasive vinegar fly, Drosophila suzukii Matsumura, has emerged as one of the most serious arthropod pests of primocane red raspberries (Rubus ideaus L.) in the United States. In raspberries, D. suzukii encounter a diverse community of microbes, including fruit rot pathogens such as Botrytis cinerea Pers and Cladosporium cladosporioides de Vries. In this study, our primary objectives were to evaluate D. suzukii–fungal associations and determine D. suzukii's influence on fungal communities in raspberry fruit. Through culture-based surveys of larval gut microbes, we isolated several yeast fungi (primarily Hanseniaspora spp.), as well as Cladosporium, Botrytis, and several other non-yeast fungi from larval frass, suggesting that D. suzukii larvae encounter and feed on these fungi. Subsequent field surveys confirmed that D. suzukii larvae occurred in berries affected by Botrytis fruit rot and Cladosporium fruit rot. Under laboratory conditions, D. suzukii may facilitate C. cladosporioides infections, likely through the introduction of epiphytic propagules on the fruit surface. We could not detect impacts on B. cinerea infections or establish a clear vectoring relationship for either fruit rot. These studies provide evidence for an association between D. suzukii and fungal fruit rot pathogens. Understanding interactions between raspberry fruit, D. suzukii, and fungal microbes—especially whether D. suzukii facilitates the development of fruit rots or conversely, if fruit rots influence D. suzukii infestation patterns—may improve pest and pathogen management programs.
Harmonia axyridis (Pallas), an invasive non-native species in central Europe, can outcompete other aphidophagous species. The distribution and abundance of H. axyridis vary depending on different host plants, and its effects on native coccinellid communities may change accordingly. The distribution and abundance of coccinellids in central Europe (50°N, 14°E) were investigated from 2010 to 2016. Coccinellids were counted at regular intervals on cereals (Avena, Hordeum, and Triticum), herbaceous plants (Matricaria and Urtica) and trees (Acer, Betula, and Tilia). Additionally, the occurrence over time of each species on these plants was assessed and used as an index of persistence. Across all years, the adults and larvae of H. axyridis were the dominant species of coccinellid on trees. However, H. axyridis was less abundant on herbaceous plants and cereals than on trees. Populations of native coccinellids and H. axyridis co-occurred on trees and persisted for the same length of time, while native coccinellids persisted longer than H. axyridis on herbaceous plants and cereals. Compared to 1976–1986, in the 2010s, the abundance of native species decreased on all plants by 50–70%. The presence of H. axyridis could be considered as a factor driving changes in the assemblages of native coccinellids.
Cactus-dominated semiarid scrubland covers 40% of Mexican territory. This ecosystem is highly dynamic and undergoes drastic changes caused by seasonality. These temporal changes influence saprophagous insect communities associated with Cactaceae species. In this study, we analyzed the beetle community associated with decayed cactus species at the Barranca de Metztitlán Biosphere Reserve in central Mexico. We compared the diversity and composition of beetle communities in rainy and dry seasons; moreover, the network architecture of cactus–beetle interactions was examined. High dominance and abundance were detected in rainy assemblages, whereas the dry season had less abundance but more ecological diversity. A nested structure was found between individual cactus species and beetle species, as well as in an intrapopulation network between fragments of the columnar cacti Isolatocereus dumortieri (Scheidw.) Backeb. (Cactaceae), and beetle species for both seasons (rainy and dry). This finding shows more generalist than specialist beetle species inhabiting cactus species. Further research is still needed to understand whether the presence of these beetle species is determined by microhabitat conditions or the abundance of prey associated with decayed cacti. This is the first step in untangling the complex interactions among cactus–beetle species involved in the decomposition process of cacti in semiarid environments. This study provides evidence of temporal shifts in abundance and diversity patterns of these beetles associated with decayed cacti; furthermore, we did not detect an influence of seasonality on the structure of cactus–beetle interactions.
The Brazilian Cerrado, a hotspot and the largest savannah in the world, has been undergoing intense changes in land use for urbanization. The creation and maintenance of urban parks and public squares is one efficient biodiversity conservation strategy in urbanized landscapes. In this study, our objective was to evaluate the potential of urban parks with native vegetation for conservation of flower chafer beetles (Coleoptera: Cetoniinae), a beetle group usually used as a bioindicator in African landscapes, in Brazilian Cerrado. We sampled Cetoniinae beetles using aerial fruit-baited traps, every 2 wk from January to December 2014 in 10 areas of Cerrado in Aquidauana, MS, Brazil. We compared the species richness, abundance, biomass, and species composition between six ‘natural reserve’ areas (outside the urban matrix) and four ‘urban park’ areas (within the urban matrix), and identified specialist species of each habitat type. A total 508 individuals of nine species were captured. The abundance, species richness, and biomass were similar between natural reserve and urban park. However, species composition differed among the habitats. Gymnetis flava (Weber) was classified as an urban park specialist, while Euphoria lurida (Fabricius), and Hoplopyga liturata (Olivier) were classified as natural reserve specialists. Our results demonstrate that urban parks conserve the abundance, biomass and species richness of flower chafer beetles in the Brazilian Cerrado. In this context, our results suggest that the maintenance of the urban park with native vegetation can be an efficient strategy for the conservation of Cetoniinae beetles in the urban matrix in the Brazilian Cerrado.
Over the last 50 yr, the geographical distribution of soybean crop production in Brazil has expanded from the southern region to Maranhão state in the north. We evaluated if this latitudinal expansion affected the community of stink bugs (Hemiptera: Pentatomidae) and their parasitoids. The fauna of stink bugs and their adult parasitoids were studied in nine soybean production regions in Brazil. Stink bugs were sampled using a shake cloth and and held in laboratory cages with natural diet to await emergence of parasitoids. Stink bug and parasitoid species composition did not shift along the latitudinal gradient. Euschistus heros (Fabricius, 1798) (Hemiptera: Pentatomidae) was the most abundant stink bug and occurred in all sampling regions. Hexacladia smithii Ashmead, 1891 (Hymenoptera: Encyrtidae), Cylindromyia brasiliana (Townsend, 1927), Ectophasiopsis sp., Eutrichopoda sp., Gymnoclytia sp., Phasia sp., and Trichopoda sp. (Diptera: Tachinidae) were the parasitoid adult stink bugs that we registered. Parasitism indexes were low, ranging from 0.77 to 6.05% through the regions. On the other hand, parasitism rates were higher in areas with reduced insecticide application in comparison to areas with intensive insecticide use.
Co-occurring plant species can influence the extent of damage to each other by altering the activity or abundance of a shared herbivore. One mechanism by which neighboring host plants exacerbate damage to a focal host is if the neighbor amplifies herbivore populations. We studied the performance of a shared herbivore on a native and an invasive plant, to estimate how strongly the presence of the invasive plant increases local herbivore abundance—in a system in which highly asymmetric spillover herbivory may occur. Specifically, we conducted a series of greenhouse experiments that measured reproduction, development, and survival of the invasive stink bug Bagrada hilaris Burmeister on an invasive annual forb, Sahara mustard (Brassica tournefortii), or a native perennial shrub, four-winged saltbush (Atriplex canescens). All measured aspects of stink bug performance revealed consistently greater performance on Br. tournefortii. Indeed, A. canescens appears to be insufficient for Ba. hilaris to complete its development. Nonetheless, preliminary damage assessments found that both plant species were used as feeding hosts, putative feeding lesions were a more reliable indicator of herbivory than was the degree of yellowing, and higher Ba. hilaris abundance was generally associated with greater sublethal damage to A. canescens. Thus, A. canescens appears to be susceptible to Ba. hilaris herbivory, though more research is needed to assess fitness impacts of this novel herbivore. Our results indicate that differential herbivore performance among host plants may be an important contributor to observed patterns of abundance of a shared herbivore and spillover herbivory between plants.
Many beetle species emerge in twigs pruned from the host tree by larvae inside the twig or externally girdled by adult females. Benefits of developing in fallen twigs have been afforded little experimental attention. If predation or parasitism in the canopy drive pruning and girdling behaviors, emergence is expected to be greatest in twigs on the ground, where predation and parasitism are expected to be minimized. Here, 220 twigs pruned from oak trees by larval Anelaphus parallelus (Newman) (Coleoptera: Cerambycidae) were randomly placed into one of four treatments in a forested hedge: 1) on the ground; 2) on the ground within a mesh bag; 3) tied into the hedge 2.5 m above the ground; 4) secured in a mesh bag and tied into the hedge; or 5) stored in a cool basement.The percentage of beetle emergence was greatest in twigs stored in the basement (87%) and bagged twigs on the ground (74%) and was least from unbagged twigs placed in the hedge (40%). Reduced rates of predation on the ground are, therefore, implicated as a potential selective force for pruning behaviors. The percentage of parasitized twigs was least from twigs stored in a basement (2%) but, unexpectedly, greatest from twigs placed in mesh bags in the hedge (24%). Support for parasitism as a determinant of pruning behavior was, therefore, ambiguous but may be confounded if mesh bags did not deter parasitoids. Considering results of other studies, selective forces for pruning and girdling behaviors may not generalize among species.
Bacterial endosymbionts, particularly Wolbachia (Rickettsiales: Rickettsiaceae), Rickettsia (Rickettsiales: Rickettsiaceae), and Cardinium (Bacteroidales: Bacteroidaceae), are commonly found in several arthropod groups, including insects. Most estimates of the global infection rate of Wolbachia (52% [95% credible intervals: 44–60]) show that these bacteria infect more than half of all insect species. Other endosymbionts, such as Rickettsia (24% [confidence intervals [CIs] 20–42]) and Cardinium (13% [CIs 13–55]), infect a smaller but still substantial proportion of insect species. In spite of these observations, it is unclear what proportion of individuals within those species are infected. Here, we used published databases to estimate the proportion of individuals that are infected with either Wolbachia, Rickettsia, or Cardinium. We found that the majority (69%) of Wolbachia-infected species have less than half of their individuals infected with Wolbachia, indicating that although the bacterium may be common among species, it is not common within species. The same was true for Rickettsia (81%) and Cardinium (87%). This discrepancy was consistent across orders, in which less than 10% of individuals were typically infected, even though more than 50% of species within orders were infected. For example, according to our model, nearly 50% of beetle (Coleoptera) species are infected with Wolbachia (i.e., contain at least one individual that has tested positive for Wolbachia), but less than 5% of all individuals are infected. These results add to the growing knowledge base about endosymbionts in insects and should guide future sampling efforts and investigations on the role that these bacteria play in populations.
The outbreak of the coconut scale insect Aspidiotus rigidus Reyne (Hemiptera: Encyrtidae) posed a serious threat to the coconut industry in the Philippines. In this article, we modeled the interaction between A. rigidus and its parasitoid Comperiella calauanica Barrion, Almarinez, Amalin (Hymenoptera: Encyrtidae) using a system of ordinary differential equations based on a Holling type III functional response. The equilibrium points were determined, and their local stability was examined. Numerical simulations showed that C. calauanica may control the population density of A. rigidus below the economic injury level.
Sugar feeding by biological control agents, such as parasitoid wasps, may enhance their ability to control crop pests, although its importance is likely to vary greatly through space and time. Here we quantified temporal variation in the potential importance of sugar resources associated with honeydew secreted by the pea aphid (Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae)) in determining levels of parasitism of the alfalfa weevil (Hypera postica (Gyllenhal) (Coleoptera: Curculionidae)) by its dominant parasitoid, Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae) across irrigated alfalfa fields in Montana, United States over 5 yr. A positive association between parasitism of H. postica and A. pisum densities at the across-site scale was observed in 2 of 5 yr, with parasitism increasing twofold to fourfold over gradients in A. pisum density. The relationship was strongest in the 2 yr of lowest parasitoid relative to host densities, when increases in per capita effects of individual parasitoids would be expected to be particularly important. Acyrthosiphon pisum densities were at their lowest in these same years, suggesting that they may generally be sufficiently abundant that parasitoids are not limited by sugars in most years. This conclusion is supported by results of anthrone tests which revealed a high level of sugar-fed parasitoids (>50%) in a year of high aphid abundance. More studies, such as this one, that explore the frequency with which increasing sugar resource availability actually enhances parasitism levels in the field will be critical to gauge the broader potential of sugar resource addition (e.g., through flowering strips, banker plants or sugar sprays) to bolster biological control.
Entomopathogenic fungi (EPF), such as Metarhizium spp. and Beauveria bassiana, are widely used in the biocontrol of many species of insect pests. Tobacco is an economically important crop in Guangdong Province of China, but insect pests, such as Spodoptera litura Fabricius, are a major threat to production. Here, we tested the persistence of five Metarhizium species and B. bassiana in glasshouse pot and field experiments and assessed their long-term efficacy against S. litura. We found that the colony forming units of these EPF decreased by c. 93% by 180 d in the pot soils declines tended to be exponential. In contrast, declines of c. 99% in field soils were more gradual (linear), occurring throughout the 360 d experiment. Metarhizium anisopliae Ma09 had the longest estimated half-life of 41 d, while that of B. bassiana was the shortest (9 d). Fungal density in the upper soil layer (0–5 cm) decreased rapidly and was undetectable after 150 d, whereas density was consistently greatest in the mid-layer (10–15 cm). At 180 d after inoculation, strain Ma09 elicited highest rates of mortality in S. litura. We conclude that soils in Guangdong Province are all suitable for the use of Metarhizium as a biocontrol agent, where M. anisopliae Ma09 offers greatest residual activity.
The effect of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin on the development of immature stages, and survival and fecundity of Coptera haywardi (Oglobin) adults was studied under laboratory conditions.The fungus was applied as dry conidia on parasitized pupae of Anastrepha obliqua (Macquart) (Diptera: Tephritidae) and on parasitoid adults of two different age groups (1- to 4-d-old, and 5- to 10-d-old). The fungus caused no negative effects on the development of the immature stages, since there were no differences on the emergence of adults compared with the untreated control. Adults were susceptible to the fungus on both sexes and age groups. Males showed shorter lifespan than females, even in untreated individuals. Despite the increased adult mortality produced by the fungus there was no effect on fecundity during first 18 d of adult life, as the net fecundity was 26.7 and 26.3 parasitoids per female treated and untreated, respectively. Our results suggest that, given the low susceptibility of parasitized pupae and the no effect on fecundity during the first 18 d of adult life, it is possible to develop management strategies using these two natural enemies in the biological control against A. obliqua.
The leaf-webber Spoladea recurvalis F. is the most devastating pest of amaranths in East Africa. Recent collaborative research in Asia and East Africa revealed one highly resistant amaranth accession (VI036227) to the pest and seven moderately resistant ones (RVI00053, VI033479, VI044437-A, VI047555-B, VI048076, VI049698, and VI056563). The solitary koinobiontic endoparasitoid Apanteles hemara Nixon has also been reported as efficient against the pest. Plant resistance to herbivores may have bottom-up effects on their parasitoids. In this study, we assessed the effects of the seven moderately resistant amaranth accessions and one susceptible accession (VI033482) on the performance of A. hemara. Except VI056563 that recorded lower parasitism rates compared to the susceptible accession, A. hemara performed well on all the other moderately resistant accessions.The longevity of the parasitoid was significantly extended on the resistant accessions compared to the susceptible one. While the parasitoid's body size, developmental time, and survival differed significantly between resistant accessions, they were similar to results obtained on the susceptible accession. Furthermore, while the parasitoid's sex ratio was male-biased in the susceptible accession, balanced sex ratios were obtained from accessions RVI00053, VI033479, VI044437-A, VI047555-B, VI048076, and VI049698. Significant nonreproductive host larval mortality was induced by A. hemara on all the tested accessions. These results suggest that the moderately resistant accessions can be used in combination with the endoparasitoid A. hemara to manage S. recurvalis and other amaranth leaf-webbers in the context of integrated pest management.
The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), is an invasive agricultural and nuisance pest that has established across much of the United States and caused significant crop losses in the Mid-Atlantic region. While it has been monitored extensively using ground-deployed pheromone traps, the vertical distribution of its life stages in the canopy of wild tree hosts has not been examined. In Virginia, small pyramid traps baited with ‘low-dose’ H. halys pheromone lures were deployed via a pulley system at the lower, mid-, and upper canopy of female tree of heaven (Ailanthus altissima (Mill.) Swingle) in 2016 and 2017 and male A. altissima and hackberry (Celtis occidentalis L.) in 2017. Weekly captures of adults and nymphs were recorded throughout each season. Each year, additional female A. altissima trees were felled during the two main periods of H. halys oviposition. The number and relative locations of all pentatomid egg masses found on foliage were recorded and any parasitoids that emerged from them were identified. Halyomorpha halys adults and nymphs were captured in greatest numbers in upper canopy traps and in lowest numbers in traps near the tree base. More H. halys egg masses were collected from mid-canopy than from the lower or upper canopy. The adventive egg parasitoid, Trissolcus japonicus (Ashmead) (Hymenoptera: Scelionidae), emerged most frequently from egg masses found at mid-canopy and was not recovered from those in the lower canopy. Results are discussed in relation to the foraging ecology of H. halys and its natural enemies, including TT. japonicus.
Invasion of Polygraphus proximus (Blandford) has caused an extensive destruction in the aboriginal forest ecosystems of South Siberia. The goal of this study was to better understand the acoustic communication of P. proximus by analyzing the beetles' sound-production mechanisms and comparing sounds produced during different behaviors. Comparisons applied waveform analysis and quantitation of temporal parameters such as syllable, chirp duration, interchirp interval, number of tooth-strike per chirp, strike rate, and the duration of intervals between strikes. We recorded the acoustic signals of the bark beetle in three behavioral contexts: stress (handling), rivalry (male–male interactions), and courtship (male–female interactions). Acoustic signals produced during stress, rivalry behavior, and courtship chirps have very similar waveforms but are distinguishable according to temporal parameters (e.g., number of strikes in chirps and duration of intervals between them). During courtship, males produce two types of chirps. The first type was produced in all three contexts.The second chirp type was registered only in male–female interactions just before copulation. Precopulation signals produced by rubbing of the tibia against the elytral margin were registered for the first time in a bark beetle. The role of the precopulation signal was the clearest. The established modulations of signals in stress trials in comparison with the similar courtship and rivalry chirps are apparently due to effects of insect body movement against restraint. We hypothesize that the chirp temporal parameters in courtship and rivalry may be used by the sender to reveal his presence or physical characteristics to a receiver (female or rival male).
During field bioassays in Kenya of 10 chemicals that are common pheromone components of cerambycid beetles, six species in the subfamily Cerambycinae were significantly attracted to 3-hydroxyhexan-2-one, and one species in the subfamily Lamiinae was significantly attracted to 2-(undecyloxy)ethanol (known as monochamol). These results further demonstrate that the former compound is highly conserved as a cerambycid pheromone because it has now been identified or implicated in the pheromones of numerous cerambycine species native to all six habitable continents. Similarly, monochamol has been identified or implicated as a pheromone component for species in the subfamily Lamiinae native to Asia, Europe, North America, and now Africa. The eight other compounds tested, including (E)-6,10-dimethyl-5,9-undecadien-2-ol (fuscumol), the corresponding (E)-6,10-dimethyl-5,9-undecadien-2-yl acetate (fuscumol acetate), syn- and anti-(2,3)-hexanediols and (2,3)-octanediols, 3-hydroxyoctan-2-one, and 3-hydroxydecan-2-one, did not attract significant numbers of any species.
The southern pine beetle, Dendroctonus frontalis Zimmermann (Coleoptera: Curculionidae: Scolytinae) utilizes a multi-component aggregation pheromone to mediate mass-attacks and thereby colonize otherwise unsusceptible trees. Females produce the attractant frontalin and a synergist, trans-verbenol. We investigated trans-verbenol to determine whether enantiomeric composition, airborne concentration, and possibly other factors might affect its biological activity. Newly-emerged females from Mississippi populations produced 54–87% of the (–)-enantiomer; females initiating galleries in logs produced lower amounts and a wider range of enantiomeric ratios [12–92% (–)]. Coupled gas chromatography-electroantennographic detection (GC-EAD) studies did not suggest large differences in the concentration threshold of olfaction for the two enantiomers. We examined the effect of adding trans-verbenol to traps located outside infested areas and baited with components of the aggregation attractant. Male attraction was similarly increased by lures with 3, 81, or 98% of the (–)-enantiomer of trans-verbenol, whereas females preferred 81 over 3%. When release rate of 81% (–)-trans-verbenol in traps was varied across three orders of magnitude (0.3, 3, and 30 mg/d), the data suggested a positive dose–response trend. A high release (i.e., 2–5 g/d) device of host-odor alpha-pinene had a much stronger enhancing effect on trap catches than a trans-verbenol device (∼30 mg/d), and trans-verbenol did not further enhance attraction when alpha-pinene was present. Our results suggest that the weak attraction-enhancing activity of trans-verbenol reported previously cannot be improved by adjusting the enantiomeric composition or release rate of lures, and furthermore there are no anticipated benefits of adding trans-verbenol to the D. frontalis monitoring lure.
Natural enemies can be important regulators of pests in agroecosystems, and they often rely on volatile chemical cues to find hosts. Herbivore-induced plant volatiles (HIPVs) have been a focal point in many studies that seek to increase the efficacy of biological control programs by increasing recruitment and retention of natural enemies. Our research sought to explore the role of HIPVs in asparagus agroecosystems to answer the following questions: 1) What is the composition of HIPV produced by asparagus ferns following feeding by a chewing herbivore? 2) Do field deployed lures baited with synthetic asparagus HIPVs attract natural enemies? and 3) Can HIPV lures increase biological control of asparagus pests? Volatiles were field collected from the headspace of healthy asparagus ferns, mechanically damaged ferns, and ferns fed upon by asparagus beetle larvae (Crioceris asparagi L.) (Coleoptera: Chrysomelidae). We found that asparagus beetle damaged asparagus had significantly higher concentrations of (E)-β-ocimene, (E,E)-α-farnesene, and (1)-tetradecanol than healthy or mechanically damaged ferns. Field experiments demonstrated that lures baited with isolates of ocimene and farnesene attracted parasitoids without attracting pests, but had no impact on predator recruitment. Finally, we determined that overall parasitism rates were not increased by synthetic HIPV lures but found evidence that lures may increase parasitism of asparagus miner (Ophiomyia simplex Loew) (Diptera: Agromyzidae) by pteromalids.
Halyomorpha halys (Stål) (Heteroptera: Pentatomidae), the brown marmorated stink bug (BMSB), is a polyphagous fruit and vegetable pest from eastern Asia and now invasive in the United States and Europe. Earlier research revealed that the main volatile from hexane egg extracts of a western North American pentatomid, Euschistus conspersus Uhler, to which two native scelionid egg parasitoids, Telenomus podisiAshmead and Trissolcus erugatus Johnson are highly attracted, was methyl (2E,4Z)-2,4-decadienoate, the major component of the conspecific male-produced aggregation pheromone. Conversely, extracts of BMSB eggs lacked the male-produced sesquiterpenoid H. halys pheromone components but contained C16,18,20 aldehydes (hexadecanal, octadecanal, and eicosanal); both egg-surface extracts of BMSB eggs and the C16,18,20 synthetic aldehyde blend repelled the female parasitoids. The goal of the present research was to manipulate egg-surface volatiles to induce the scelionid egg parasitoids to adopt BMSB eggs as a host. Here it was demonstrated that individual females of both parasitoids could be conditioned to H. halys egg-surface aldehydes inY-tube olfactometer experiments, and this positive memory lasted 3–4 d. Furthermore, conditioned wasps successfully parasitized fresh H. halys eggs in no choice tests, and their offspring continued to successfully parasitize fresh H. halys eggs for 2–3 more generations. Eventually, both the individual and generational memories faded. Unconditioned female parasitoids were not attracted to H. halys egg extract or the synthetic blend of egg-surface aldehydes, nor did they parasitize BMSB eggs.Theoretical and practical implications of the research are discussed in the contexts of Hopkins' host selection principle, biological control, and instinct evolution.
The macadamia felted coccid, Eriococcus ironsidei (Williams) is an invasive pest of macadamia orchards that causes severe damage to the trees and reduces nut yield in Hawaii. Their feeding results in distortion and stunting of new growth, and with high population densities, dieback of entire branches may result. Ten macadamia orchards were sampled on the Hawaii island over a period of 18 mo to characterize the dispersion of the pest in the field, and to use those data as the basis for the development of a binomial sampling plan. Analyses based on Taylor's Power Law and Iwao's mean crowding index indicated an aggregated pattern of dispersion of the pest in the field. Curvilinear relationships between mean crawler density and the proportion of infested trees based on four tally thresholds (crawlers per unit area, T > 0, 5, 10, 20) were plotted. Results showed that a tally threshold T > 10 was the best predictor to model mean crawler density. Binomial sequential sampling plans based on three critical proportions of trees infested (0.40, 0.60, and 0.80) were developed. The adoption of a binomial sequential sampling plan for use in decision making can contribute to improve the management of E. ironsidei and optimize the number of samples needed to make decisions to control this pest.
Knowledge of the diversity of fruit flies is essential for understanding aspects of their community ecology. However, the effectiveness of sampling methods in representing species diversity and relationships with hosts in a diverse environment has not been adequately assessed. This study aimed to determine the optimum method to represent the diversity of fruit flies and assess their relationships with host fruits. Species of Anastrepha sampled with both traps and fruits in the same area were comprehensively analyzed. Data were analyzed by Hill's numbers (species diversity in both sampling methods), heat map graph (interaction of species with methods), and rank clocks (population fluctuations of the most abundant species). We also measured the interaction strength of the species. Our results showed that estimated parameters of species diversity in an area may differ when sampled with traps or fruits. However, the most abundant species appeared to interact similarly in both methods. Fruits of members of the families Myrtaceae and Anacardiaceae contributed highly to the presence of Anastrepha. The optimum strategy to represent Anastrepha diversity in an area is the combined use of both sampling methods.
A phenology model of the walnut husk fly, Rhagoletis completa Cresson, was developed to more accurately predict the timing of the flight period and optimize management decisions. A data set of 153 orchard years in which adults were trapped throughout the season was used for the development and validation of this model. Data from California Irrigation Management Information System (CIMIS) weather stations were used to match orchard-year datasets with historical climatic data on degree-day (DD) accumulation, winter chill, and winter rainfall. A cumulative Weibull distribution was used to model the relationship between cumulative trap catch and DD accumulation for R. completa in California. The model was used to predict thermal requirements for the start (5% cumulative trap catch) and mid-point (50% cumulative trap catch) of the flight period, which were 1,670 and 2,179 DDs, respectively. The prediction for 50% cumulative trap catch of R. completa in California was much higher than the thermal requirement estimated in Oregon previously (1,751 DDs). Linear mixed effects models were used to evaluate other environmental and orchard-specific factors which could explain the large variation between predicted and observed thermal requirements for both the start and mid-point of the flight period. Latitude, walnut cultivar leaf-out time, orchard age and year, as a continuous variable, all contributed significantly to explain deviations from the predictions of the DD model for individual orchard years. Such factors can be used both to adjust predicted thermal requirements for these two specific and informative stages of the flight period, and to provide a basis for ecological and evolutionary hypotheses.
For insects, odorant-binding proteins (OBPs) play an essential role in binding and transporting semiochemicals through the sensillum lymph to olfactory receptor neurons within the antennal sensilla. In the present study, the full-length cDNA encoding a general odorant-binding protein 1 (DcitOBP1, accession number KY475564) was cloned from the antennae of Diaphorina citri using RACE-PCR, and qRT-PCR analysis revealed that the DcitOBP1 gene was expressed mainly in the antennae of D. citri. In molecular docking assay, the results showed that DcitOBP1 protein has better binding affinities to the 12 selected host-plant volatile compounds. Then, the recombinant DcitOBP1 protein was expressed in Escherichia coli. After removed His-Tag, the binding properties of purified DcitOBP1 protein to the selected host-plant volatile compounds were investigated in a fluorescence ligand-binding assay, similar, but more obviously binding properties of DcitOBP1 protein result were obtained, the dissociation constant (KD) value of DcitOBP1/1-NPN complex was 6.440 ± 0.521, and the DcitOBP1 protein showed high binding affinities (IC50 < 100 μM) to six of the selected ligands, namely methyl salicylate, α-phellandrene, (1R)-(+)-α-pinene, 3-carene, β-caryophyllene, and α-caryophyllene. Additionally, the behavior bioassays were also showed that D. citri had significant behavioral responses toward to α-caryophyllene, β-caryophyllene, (1R)-(+)-α-pinene, and α-phellandrene. Our investigation infer that the DcitOBP1 protein might play a crucial role in host-plant volatile odorants' perception in D. citri, and these results also have been supplied previous insight evidence into the physiological functions of the DcitOBP1 protein of D. citri.
Jessica Pérez-Alquicira, Esther van der Knaap, Kristin Mercer, Leah McHale, Thomas Mitchell, Jose Luna-Ruiz, Esther Texocotitla-Vázquez, Ofelia Vargas-Ponce, Andy Michel
Host-associated differentiation (HAD) has played a major role in insect diversification at both macroevolutionary and microevolutionary scales.This evolutionary process has been reported in insects associated with wild and domesticated plant species. In particular, domesticated species harbor large genetic and phenotypic diversity associated with traits of human interest, including variation in nutrition, phenology, fruit, and leaf shape.This diversity may alter selection regimes affecting insect evolution and host specialization.The genus Liriomyza includes highly polyphagous species that are characterized for living and feeding inside plant leaves. Ecological and genetic data suggest the presence of cryptic species within this genus. Moreover, there is evidence of HAD in a group of populations of Liriomyza trifolii (Burgess) associated with Capsicum annum L. (Solanaceae). In this work, we explored HAD in L. trifolii populations from southeastern Mexico, and inquire into differentiation specific to peppers based on cytochrome oxidase I. We also evaluated the relationship between the genetic structure of leafminers and the different types of C. annuum. Our main results did not support previous findings of specialization of L. trifolli on C. annuum. Nevertheless, we found a divergent group of haplotypes associated to Allium cepa (Aspargales: Amaryllidaceae) in sympatric condition to Physalis philadelphica Lam. (Solanales: Solanaceae) and C. annum, suggesting the presence of HAD, as well as significant genetic differentiation of L. trifolii associated to peppers from Oaxaca and Yucatán.
Nontarget soil fauna in fields planted with transgenic Bt crops may be influenced by the Bt protein following crop establishment. Here, we investigated the effects of transgenic Cry1Ac corn Bt-799 on soil Collembola using both taxonomic and trait-based approaches in an experimental field in northeast China from 2014 to 2015. The relationship between the collembolan community and environmental variables (including corn type) was investigated using redundancy analysis (RDA). In May 2015, we found that collembolan species richness, Shannon–Wiener's index, and all trait values examined in transgenic Cry1Ac corn (Event Bt-799, Bt corn) were lower than in its near isoline (Zheng 58, non-Bt corn). However, this significant influence did not persist in the subsequent corn growth period. For all other sampling periods over 2-yr study, all indices based on taxonomic (abundance, species richness, and Shannon–Wiener's index) and trait-based (number of ocelli, body size, pigmentation, furcula development, and antennae length) approaches in Bt corn were not significantly different from non-Bt corn. The results showed no significant difference between the two corn types in the repeated-measures analysis of variance (ANOVA). Moreover, redundancy analysis (RDA) showed that corn type only explained 1% of the variation in the collembolan community. These results suggested that Bt corn did not affect collembolan community characteristics in the short term.
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